For a glimpse of the power of sexual selection, the dance of the golden-collared manakin is hard to beat. Each June in the rainforests of Panama, the sparrow-size male birds gather to fluff their brilliant yellow throats, lift their wings, and clap them together in rapid fire, up to 60 times a second. When a female favors a male with her attention, he follows up with acrobatic leaps, more wing snaps, and perhaps a split-second, twisting backflip. “If manakins were human, they would be among the greatest artists, athletes, and socialites in our society,” says Ignacio Moore, an integrative organismal biologist at Virginia Polytechnic Institute and State University.
As biologists have understood since Charles Darwin, such exhibitionism evolves when females choose to mate with males that have the most extravagant appearances and displays—a proxy for fitness. And now, by studying the genomes of the golden-collared manakin (Manacus vitellinus) and its relatives, researchers are exploring the genes that drive these elaborate behaviors and traits. Last month at the virtual meeting of the Society for Integrative and Comparative Biology, Moore and other researchers introduced four manakin genomes, adding to two already published, and singled out genes at work in the birds’ muscles and brains that may make the displays possible.
The work offers “a better understanding of why manakins do all the amazing things that they do,” says Emily DuVal, a behavioral ecologist at Florida State University. Over the past decade, researchers have learned much about how natural selection affects genomes. “In contrast, we know very little about the underlying basis of sexually selected traits,” says Christopher Balakrishnan, an evolutionary biologist at East Carolina University (ECU). By mapping traits and genes onto the manakin family tree, researchers are beginning to trace the stepwise genetic changes that led to the most elaborate displays and determine whether sexual selection works differently from natural selection.
Other species—birds of paradise and bowerbirds, in particular—also mount impressive sexual displays. But manakins have a greater variety of such traits and, being more abundant and more accessible, are easier to study in-depth. We can “assess the genomic basis for these behaviors in a way that isn’t possible for many other complex behavioral traits in vertebrates,” says Morgan Wirthlin, an evolutionary neurobiologist at Carnegie Mellon University.
As Balakrishnan and his colleagues reported at the meeting, a sweet tooth—or beak—may have set the stage for sexual selection in manakins. Their ancestors are known to have switched their diet from insects to fruit, and researchers suspected the change to a more available and abundant food source gave males extra energy for procuring mates.
By comparing genomes of manakin relatives that continue to eat insects with those of fruit-eating manakins, Balakrishnan, Maude Baldwin from the Max Planck Institute for Ornithology, and colleagues found evidence that fruit eating and elaborate male displays evolved in steps. The researchers learned that the genes coding for a savory taste receptor began to change even before manakins became fruit eaters. By the time the saffron-crested tyrant-manakin (Neopelma chrysocephalum) evolved, Baldwin reported at the meeting, the receptor had become sensitive to the sweetness of ripe fruits—a trait rare among birds. That species courts with simple hops—partway to the elaborate displays of the fruit-eating species that evolved later.
Wirthlin and others explored the DNA that changed to make those behaviors possible. In her analysis of five manakin genomes, she focused on ultraconserved noncoding elements, segments of DNA that have stayed almost exactly the same across animals ranging from chickens to humans and are thought to play a crucial role in regulating other genes. Given this conservation, she thought they’d be a good place to look for possible fingerprints of sexual selection.
In the manakin genomes, 57 elements showed slight differences from the matching sequences in other species; those changes might alter the activity of the genes they regulate. Some of those elements are clustered around genes for muscle proteins and hormone receptors and some are near genes expressed in the brain, including two, TLE4 and MEIS2, active in a region needed for fast visual processing. Both genes are less active in manakins than in zebra finches, Wirthlin reported—a change that might help male manakins cope with the visual demands of their frenetic dances.
Matthew Fuxjager, an integrative biologist at Brown University, is excited about Wirthlin’s finding that evolution may have revved up the activity of genes for the birds’ hormone receptors. The high-speed wing clapping in some species requires extra fast and powerful wing pectoral muscles—which are highly sensitive to the male hormone androgen. “Androgens are what dial up the speed,” by changing the activity of muscle performance genes, Fuxjager says.
At the meeting, Balakrishnan reported pinpointing other genes that may also have supercharged those crucial muscles. His genomic analysis suggested that the activity of genes involved in muscle metabolism and growth changed early in manakin evolution, yielding more powerful muscles. He has not looked in females, but he and Fuxjager think the demands of flight, not mating, may have driven those early changes. Then, as sexual selection began to act on later-evolving species, changes in the androgen receptors and other signaling paths made the flight muscles in males capable of the very fast movements needed for the courtship displays. (Other research shows female muscles are not as sensitive to androgens.)
The manakins’ performance involves more than sound and movement—in some species it’s a social act as well, coordinated among as many as 20 males. In all vertebrates, a network of brain “nuclei”—clusters of similar nerve cells—helps control social behavior, and studies presented at the meeting show the pattern of gene activity in those nuclei varies with testosterone levels. The work, by evolutionary biologist Peri Bolton at ECU and ecologists Brent Horton at Millersville University and Brant Ryder at the Smithsonian National Zoological Park, suggests changes in androgen receptors could have aided the birds’ social sophistication as well as their athleticism.
Dazzling as the manakins’ displays are, researchers are just as awed by their intricate genetic underpinnings. “Our studies are teaching us that beauty is more than skin deep,” Moore says.
sciencemag.org, 3 March 2021